ABA- and ET-induced systemic and intergenerational resistance against rice root-knot nematodes converges on OsMPK5-dependent signaling

Phytohormones play essential roles in plant-nematode interactions through complex crosstalk. Although these hormones often accumulate in nematode-resistant plants, the roles of abscisic acid (ABA) and ethylene (ET) in rice (Oryza sativa) resistance to the root-knot nematode (RKN) Meloidogyne graminicola (Mg) remain unclear, particularly regarding concentration dependency and underlying mechanisms. Using exogenous hormone gradient treatments, we show that only high concentrations of ABA (200 µM) and ET-releasing compound ethephon (Eth, 500 µM) induce systemic nematode resistance. High-concentration ET triggers endogenous systemic accumulation of ET and jasmonic acid (JA), accompanied by transient suppression followed by delayed accumulation of ABA, and induces JA-, ABA-, and salicylic acid (SA)-associated transcriptional responses. Exogenous ABA leads to endogenous ABA and SA accumulation and increased expression of related genes, while it suppresses ET biosynthesis gene expression and levels, highlighting a negative feedback effect of ABA on ET. Both hormones converge on a common mitogen-activated protein kinase 5 (OsMPK5)-dependent transcriptional and translational module. Low doses of ABA (50 µM) failed to activate this module and induced plant susceptibility, highlighting a threshold requirement for immune activation. Offspring of rice plants treated bi-weekly with high doses of ABA or ET were less susceptible to nematodes. This intergenerational acquired resistance was also OsMPK5-dependent. Our findings reveal concentration-dependent systemic effects of ABA and ET, whereby high-dose ABA and ET converge on OsMPK5 to reprogram translation and defense gene expression, underpinning both immediate and heritable resistance to root-knot nematodes.